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Title: Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction

Abstract

The bioreduction of Fe(III) oxides by dissimilatory iron-reducing bacteria may result in the formation of a suite of Fe(II)-bearing secondary minerals, including magnetite (a mixed Fe(II)/Fe(III) oxide), siderite (Fe(II) carbonate), vivianite (Fe(II) phosphate), chukanovite (ferrous hydroxy carbonate), and green rusts (mixed Fe(II)/Fe(III) hydroxides). In an effort to better understand the factors controlling the formation of specific Fe(II)-bearing secondary minerals, we examined the effects of Fe(III) oxide mineralogy, phosphate concentration, and the availability of an electron shuttle (9,10-anthraquinone-2,6-disulfonate, AQDS) on the bioreduction of a series of Fe(III) oxides (akaganeite, feroxyhyte, ferric green rust, ferrihydrite, goethite, hematite, and lepidocrocite) by Shewanella putrefaciens CN32, and the resulting formation of secondary minerals, as determined by X-ray diffraction, Mössbauer spectroscopy, and scanning electron microscopy. The overall extent of Fe(II) production was highly dependent on the type of Fe(III) oxide provided. With the exception of hematite, AQDS enhanced the rate of Fe(II) production; however, the presence of AQDS did not always lead to an increase in the overall extent of Fe(II) production and did not affect the types of Fe(II)-bearing secondary minerals that formed. The effects of the presence of phosphate on the rate and extent of Fe(II) production were variable among the Fe(III) oxides, butmore » in general, the highest loadings of phosphate resulted in decreased rates of Fe(II) production, but ultimately higher levels of Fe(II) than in the absence of phosphate. In addition, phosphate concentration had a pronounced effect on the types of secondary minerals that formed; magnetite and chukanovite formed at phosphate concentrations of ≤1 mM (ferrihydrite), <~100 µM (lepidocrocite), 500 µM (feroxyhyte and ferric green rust), while green rust, or green rust and vivianite, formed at phosphate concentrations of 10 mM (ferrihydrite), ≥100 µM (lepidocrocite), and 5 mM (feroxyhyte and ferric green rust). These results further demonstrate that the bioreduction of Fe(III) oxides, and accompanying Fe(II)-bearing secondary mineral formation, is controlled by a complex interplay of mineralogical, geochemical, and microbiological factors.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4]; ORCiD logo [1]
+ Show Author Affiliations
  1. Argonne National Lab. (ANL), Argonne, IL (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States); Bulgarian Academy of Sciences, Sofia (Bulgaria)
  3. Univ. of Iowa, Iowa City, IA (United States); Pennsylvania State Univ., University Park, PA (United States)
  4. Univ. of Iowa, Iowa City, IA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1777187
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Minerals
Additional Journal Information:
Journal Volume: 11; Journal Issue: 2; Journal ID: ISSN 2075-163X
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; chukanovite; dissimilatory iron reduction; green rust; iron oxide; magnetite; siderite; vivianite

Citation Formats

O’Loughlin, Edward J., Boyanov, Maxim I., Gorski, Christopher A., Scherer, Michelle M., and Kemner, Kenneth M. Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction. United States: N. p., 2021. Web. doi:10.3390/min11020149.
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O’Loughlin, Edward J., Boyanov, Maxim I., Gorski, Christopher A., Scherer, Michelle M., & Kemner, Kenneth M. Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction. United States. https://doi.org/10.3390/min11020149
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O’Loughlin, Edward J., Boyanov, Maxim I., Gorski, Christopher A., Scherer, Michelle M., and Kemner, Kenneth M. Sun . "Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction". United States. https://doi.org/10.3390/min11020149. https://www.osti.gov/servlets/purl/1777187.
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@article{osti_1777187,
title = {Effects of Fe(III) Oxide Mineralogy and Phosphate on Fe(II) Secondary Mineral Formation during Microbial Iron Reduction},
author = {O’Loughlin, Edward J. and Boyanov, Maxim I. and Gorski, Christopher A. and Scherer, Michelle M. and Kemner, Kenneth M.},
abstractNote = {The bioreduction of Fe(III) oxides by dissimilatory iron-reducing bacteria may result in the formation of a suite of Fe(II)-bearing secondary minerals, including magnetite (a mixed Fe(II)/Fe(III) oxide), siderite (Fe(II) carbonate), vivianite (Fe(II) phosphate), chukanovite (ferrous hydroxy carbonate), and green rusts (mixed Fe(II)/Fe(III) hydroxides). In an effort to better understand the factors controlling the formation of specific Fe(II)-bearing secondary minerals, we examined the effects of Fe(III) oxide mineralogy, phosphate concentration, and the availability of an electron shuttle (9,10-anthraquinone-2,6-disulfonate, AQDS) on the bioreduction of a series of Fe(III) oxides (akaganeite, feroxyhyte, ferric green rust, ferrihydrite, goethite, hematite, and lepidocrocite) by Shewanella putrefaciens CN32, and the resulting formation of secondary minerals, as determined by X-ray diffraction, Mössbauer spectroscopy, and scanning electron microscopy. The overall extent of Fe(II) production was highly dependent on the type of Fe(III) oxide provided. With the exception of hematite, AQDS enhanced the rate of Fe(II) production; however, the presence of AQDS did not always lead to an increase in the overall extent of Fe(II) production and did not affect the types of Fe(II)-bearing secondary minerals that formed. The effects of the presence of phosphate on the rate and extent of Fe(II) production were variable among the Fe(III) oxides, but in general, the highest loadings of phosphate resulted in decreased rates of Fe(II) production, but ultimately higher levels of Fe(II) than in the absence of phosphate. In addition, phosphate concentration had a pronounced effect on the types of secondary minerals that formed; magnetite and chukanovite formed at phosphate concentrations of ≤1 mM (ferrihydrite), <~100 µM (lepidocrocite), 500 µM (feroxyhyte and ferric green rust), while green rust, or green rust and vivianite, formed at phosphate concentrations of 10 mM (ferrihydrite), ≥100 µM (lepidocrocite), and 5 mM (feroxyhyte and ferric green rust). These results further demonstrate that the bioreduction of Fe(III) oxides, and accompanying Fe(II)-bearing secondary mineral formation, is controlled by a complex interplay of mineralogical, geochemical, and microbiological factors.},
doi = {10.3390/min11020149},
journal = {Minerals},
number = 2,
volume = 11,
place = {United States},
year = {Sun Jan 31 00:00:00 EST 2021},
month = {Sun Jan 31 00:00:00 EST 2021}
}
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Influence of phosphate species on green rust I transformation and local structure and morphology of γ-FeOOH
journal, August 2011

Green Rust Formation from the Bioreduction of γ –FeOOH (Lepidocrocite): Comparison of Several Shewanella Species
journal, July 2007

  • O'Loughlin, Edward J.; Larese-Casanova, Phil; Scherer, Michelle
  • Geomicrobiology Journal, Vol. 24, Issue 3-4
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Quinone Moieties Act as Electron Acceptors in the Reduction of Humic Substances by Humics-Reducing Microorganisms
journal, October 1998

  • Scott, Durelle T.; McKnight, Diane M.; Blunt-Harris, Elizabeth L.
  • Environmental Science & Technology, Vol. 32, Issue 19
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Treatment of radioactive wastes: An X-ray absorption spectroscopy study of the reaction of technetium with green rust
journal, December 2003

  • Pepper, Sarah E.; Bunker, Debbie J.; Bryan, Nicholas D.
  • Journal of Colloid and Interface Science, Vol. 268, Issue 2
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XAFS Investigation of the Interactions of U VI with Secondary Mineralization Products from the Bioreduction of Fe III Oxides
journal, March 2010

  • O’Loughlin, Edward J.; Kelly, Shelly D.; Kemner, Kenneth M.
  • Environmental Science & Technology, Vol. 44, Issue 5
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The mineralogic transformation of ferrihydrite induced by heterogeneous reaction with bioreduced anthraquinone disulfonate (AQDS) and the role of phosphate
journal, November 2011

  • Zachara, John M.; Kukkadapu, Ravi K.; Peretyazhko, Tanya
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 21
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Formation of tabular single-domain magnetite induced by Geobacter metallireducens GS-15
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  • Vali, H.; Weiss, B.; Li, Y. -L.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 46
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Cell adhesion of Shewanella oneidensisto iron oxide minerals: Effect of different single crystal faces
journal, December 2005

  • Neal, Andrew L.; Bank, Tracy L.; Hochella, Michael F.
  • Geochemical Transactions, Vol. 6, Issue 4
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Role of phosphate species during the formation and transformation of the Fe(II–III) hydroxycarbonate green rust
journal, May 2007

  • Refait, Ph.; Reffass, M.; Landoulsi, J.
  • Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 299, Issue 1-3
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Effects of Phosphate on Secondary Mineral Formation During the Bioreduction of Akaganeite (.β-FeOOH): Green Rust Versus Framboidal Magnetite
journal, July 2015

Influence of humic acid imposed changes of ferrihydrite aggregation on microbial Fe(III) reduction
journal, May 2012

Ferrous hydroxy carbonate is a stable transformation product of biogenic magnetite
journal, February 2005

The Influence of Carbon Source on the Products of Dissimilatory Iron Reduction
journal, September 2009

  • Salas, Everett Cossio; Berelson, William M.; Hammond, Douglas E.
  • Geomicrobiology Journal, Vol. 26, Issue 7
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Magnetite as a precursor for green rust through the hydrogenotrophic activity of the iron-reducing bacteria Shewanella putrefaciens
journal, December 2015

  • Etique, M.; Jorand, F. P. A.; Ruby, C.
  • Geobiology, Vol. 14, Issue 3
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Orenia metallireducens sp. nov. Strain Z6, a Novel Metal-Reducing Member of the Phylum Firmicutes from the Deep Subsurface
journal, August 2016

  • Dong, Yiran; Sanford, Robert A.; Boyanov, Maxim I.
  • Applied and Environmental Microbiology, Vol. 82, Issue 21
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In situ Mössbauer spectroscopy: Evidence for green rust (fougerite) in a gleysol and its mineralogical transformations with time and depth
journal, September 2005

  • Feder, Frédéric; Trolard, Fabienne; Klingelhöfer, Göstar
  • Geochimica et Cosmochimica Acta, Vol. 69, Issue 18
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Characterization and Description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an Aryl-Halorespiring Facultative Anaerobic Myxobacterium
journal, February 2002

Effect of Phosphate on the Formation of Nanophase Lepidocrocite from Fe(II) Sulfate
journal, January 2000

Degeneration of biogenic superparamagnetic magnetite
journal, January 2009

Reductive Dechlorination of Carbon Tetrachloride Using Iron(II) Iron(III) Hydroxide Sulfate (Green Rust)
journal, January 1999

  • Erbs, Marianne; Bruun Hansen, Hans Christian; Olsen, Carl Erik
  • Environmental Science & Technology, Vol. 33, Issue 2
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Archaea catalyze iron-dependent anaerobic oxidation of methane
journal, October 2016

  • Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 45
  • DOI: 10.1073/pnas.1609534113

Abiotic Reductive Dechlorination of Chlorinated Ethylenes by Iron-Bearing Soil Minerals. 2. Green Rust
journal, December 2002

  • Lee, Woojin; Batchelor, Bill
  • Environmental Science & Technology, Vol. 36, Issue 24
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Ferrous phosphate surface precipitates resulting from the reduction of intragrain 6-line ferrihydrite by Shewanella oneidensis MR-1
journal, July 2010

  • Peretyazhko, T. S.; Zachara, J. M.; Kennedy, D. W.
  • Geochimica et Cosmochimica Acta, Vol. 74, Issue 13
  • DOI: 10.1016/j.gca.2010.04.008

Influence of silicate ions on the formation of goethite from green rust in aqueous solution
journal, July 2007

Identification of Green Rust in Groundwater
journal, May 2009

  • Christiansen, B. C.; Balic-Zunic, T.; Dideriksen, K.
  • Environmental Science & Technology, Vol. 43, Issue 10
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Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: A linear free energy relationship
journal, September 2009

  • Bonneville, Steeve; Behrends, Thilo; Van Cappellen, Philippe
  • Geochimica et Cosmochimica Acta, Vol. 73, Issue 18
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Green rust formation controls nutrient availability in a ferruginous water column
journal, July 2012

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  • Geology, Vol. 40, Issue 7
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Dependence of Secondary Mineral Formation on Fe(II) Production from Ferrihydrite Reduction by Shewanella oneidensis MR-1
journal, March 2018

Mineral transformations associated with goethite reduction by Methanosarcina barkeri
journal, September 2011

Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens
journal, July 2009

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  • Geochimica et Cosmochimica Acta, Vol. 73, Issue 14
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Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer
journal, October 1999

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  • International Journal of Systematic Bacteriology, Vol. 49, Issue 4
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Reactivity of Fe(II)-Bearing Minerals toward Reductive Transformation of Organic Contaminants
journal, February 2004

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  • Environmental Science & Technology, Vol. 38, Issue 3
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The Synthesis of Green Rust II(Fe III 1 –Fe II 2 ) and Its Spontaneous Transformation into Fe 3 O 4
journal, September 1984

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  • Bulletin of the Chemical Society of Japan, Vol. 57, Issue 9
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Phosphorus dynamics in soils and landscapes
journal, December 1985

Reduction of SeO 4 2 - Anions and Anoxic Formation of Iron(II)−Iron(III) Hydroxy-Selenate Green Rust
journal, March 2000

  • Refait, Philippe; Simon, Lilian; Génin, Jean-Marie R.
  • Environmental Science & Technology, Vol. 34, Issue 5
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The mechanisms of reduction of hexavalent chromium by green rust sodium sulphate: Formation of Cr-goethite
journal, July 2006

  • Skovbjerg, L. L.; Stipp, S. L. S.; Utsunomiya, S.
  • Geochimica et Cosmochimica Acta, Vol. 70, Issue 14
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X-ray absorption and photoelectron spectroscopy investigation of selenite reduction by FeII-bearing minerals
journal, December 2008

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Phosphate loading alters schwertmannite transformation rates and pathways during microbial reduction
journal, March 2019

Fougerite, a new mineral of the pyroaurite-iowaite group: description and crystal structure
journal, June 2007

  • Trolard, Fabienne; Bourrié, Guilhem; Abdelmoula, Mustapha
  • Clays and Clay Minerals, Vol. 55, Issue 3
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Fougerite: the not so simple progenitor of the first cells
journal, October 2019

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  • Interface Focus, Vol. 9, Issue 6
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Abiotic reduction of nitro aromatic pesticides in anaerobic laboratory systems
journal, January 1989

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  • Journal of Agricultural and Food Chemistry, Vol. 37, Issue 1
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Mössbauerite, Fe 6 3+ O 4 (OH) 8 [CO 3 ]·3H 2 O, the fully oxidized ‘green rust’ mineral from Mont Saint-Michel Bay, France
journal, April 2014

Reduction of Fe(III) (Hydr)oxides with Known Thermodynamic Stability by Geobacter metallireducens
journal, June 2004

Biotransformation of two-line silica-ferrihydrite by a dissimilatory Fe(III)-reducing bacterium: formation of carbonate green rust in the presence of phosphate
journal, July 2004

  • Kukkadapu, Ravi K.; Zachara, John M.; Fredrickson, James K.
  • Geochimica et Cosmochimica Acta, Vol. 68, Issue 13
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BIOGEOCHEMICAL AND ENVIRONMENTAL FACTORS IN Fe BIOMINERALIZATION: MAGNETITE AND SIDERITE FORMATION
journal, February 2003

Biotransformation of lepidocrocite in the presence of quinones and flavins
journal, August 2013

Green rust as a precursor for magnetite: an in situ synchrotron based study
journal, February 2008

Enhancement of Hematite Bioreduction by Natural Organic Matter
journal, July 2002

  • Royer, Richard A.; Burgos, William D.; Fisher, Angela S.
  • Environmental Science & Technology, Vol. 36, Issue 13
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Fe(II)/Fe(III) ‘green rust’ developed within ochreous coal mine drainage sediment in South Wales, UK
journal, December 2006

Observations and assessment of iron oxide and green rust nanoparticles in metal-polluted mine drainage within a steep redox gradient
journal, January 2014

  • Johnson, Carol A.; Freyer, Gina; Fabisch, Maria
  • Environmental Chemistry, Vol. 11, Issue 4
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Reaction of Uranium(VI) with Green Rusts: Effect of Interlayer Anion
journal, July 2015

Neptunyl (Np) interaction with green rust,
journal, March 2011

  • Christiansen, B. C.; Geckeis, H.; Marquardt, C. M.
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 5
  • DOI: 10.1016/j.gca.2010.12.003

Arsenic sequestration by sorption processes in high-iron sediments
journal, December 2007

  • Root, Robert A.; Dixit, Suvasis; Campbell, Kate M.
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 23
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Characterization of Predominant Reductants in an Anaerobic Leachate-Contaminated Aquifer by Nitroaromatic Probe Compounds
journal, January 1998

  • Rügge, Kirsten; Hofstetter, Thomas B.; Haderlein, Stefan B.
  • Environmental Science & Technology, Vol. 32, Issue 1
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Kinetics of Cr(VI) Reduction by Carbonate Green Rust
journal, September 2001

  • Williams, Aaron G. B.; Scherer, Michelle M.
  • Environmental Science & Technology, Vol. 35, Issue 17
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Controls on Iron Reduction and Biomineralization over Broad Environmental Conditions as Suggested by the Firmicutes Orenia metallireducens Strain Z6
journal, July 2020

  • Dong, Yiran; Sanford, Robert A.; Boyanov, Maxim I.
  • Environmental Science & Technology, Vol. 54, Issue 16
  • DOI: 10.1021/acs.est.0c03853

Electron Donor Utilization and Secondary Mineral Formation during the Bioreduction of Lepidocrocite by Shewanella putrefaciens CN32
journal, July 2019

  • O’Loughlin, Edward J.; Gorski, Christopher A.; Flynn, Theodore M.
  • Minerals, Vol. 9, Issue 7
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Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones
journal, February 2002

Coprecipitation of Fe(II–III) hydroxycarbonate green rust stabilised by phosphate adsorption
journal, January 2004

Thermoterrabacterium ferrireducens gen. nov., sp. nov., a Thermophilic Anaerobic Dissimilatory Fe(III)-Reducing Bacterium from a Continental Hot Spring
journal, April 1997

  • Slobodkin, A.; Reysenbach, A. -L.; Strutz, N.
  • International Journal of Systematic Bacteriology, Vol. 47, Issue 2
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Abiotic reduction of uranium by Fe(II) in soil
journal, August 2012

Phosphate Imposed Limitations on Biological Reduction and Alteration of Ferrihydrite
journal, January 2007

  • Borch, Thomas; Masue, Yoko; Kukkadapu, Ravi K.
  • Environmental Science & Technology, Vol. 41, Issue 1
  • DOI: 10.1021/es060695p
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